Molecular Circuits That Regulate Segmentation

In the cascade of gene activity that generates the segmental pattern of the embryo (Fig. 2), segmentation proceeds by a progressive refinement of positional information that will eventually specify groups of cells that form metameric units. Refinement is initiated with maternally provided proteins that form gradients from the anterior to the posterior of the egg and early cleavage stages. These gradients of maternal proteins provide the coordinates that position the front and

FIGURE 3 Double gradients. (A) Leafhopper embryo consists of head (red), thoracic (white), and abdominal segments (black). Posterior pole of the egg is marked by bacterial symbiont (green). (B) After early egg ligation, anterior and posterior fragments form fewer segments than in the normal embryo. (C) Late ligations result in more segments formed in anterior and posterior fragments. (D) Finally, when posterior material has been displaced anteriorly and the egg ligated just below the symbiont marker a mirror-image duplication was formed. Schematic of corresponding anterior (blue) and posterior (red) gradients and their overlap (yellow) below images illustrates possible anterior and posterior gradients and their interactions in each experimental intervention.

FIGURE 3 Double gradients. (A) Leafhopper embryo consists of head (red), thoracic (white), and abdominal segments (black). Posterior pole of the egg is marked by bacterial symbiont (green). (B) After early egg ligation, anterior and posterior fragments form fewer segments than in the normal embryo. (C) Late ligations result in more segments formed in anterior and posterior fragments. (D) Finally, when posterior material has been displaced anteriorly and the egg ligated just below the symbiont marker a mirror-image duplication was formed. Schematic of corresponding anterior (blue) and posterior (red) gradients and their overlap (yellow) below images illustrates possible anterior and posterior gradients and their interactions in each experimental intervention.

back of the embryo; hence the genes that encode these proteins are called the maternal coordinate genes. The function of these maternal gradients is to activate the gap genes, which are so named because when their function is lacking, the segmental pattern of the embryo has large gaps in it (e.g., the three thoracic segments may be missing, or the first few abdominal segments.

The proteins encoded by the gap genes in turn activate the pair-rule genes. The pair-rules genes are expressed in every other segment and represent the first apparent metameric pattern. It was somewhat surprising that the first metameres produced by the pair-rule genes during embryogenesis do not correspond to the adult segments, but rather consist of a unit with double-segment periodicity. When pair-rule genes are absent, the larva has only half the normal number of segments. The pair-rule proteins then activate the segment polarity genes, a set of genes expressed in a segmentally reiterated manner. Finally, the homeotic genes are activated in a region-specific manner. The homeotic genes are a well-studied group of genes that are responsible for conferring segment character. They provide information on whether an individual segment will be a specific mouthpart, thoracic, or abdominal segment.

Much of what has been learned about the molecular process of segmentation is from Drosophila; how much is representative of a general process for all insects is not yet known. The segment polarity and homeotic genes, as well as their presumed functions, seem to be conserved in all insects examined so far; however, the activity of the maternal coordinate, gap, and pair-rule genes is more variable (Fig. 4). Because of the variation in the formation of germ anlage, it is not surprising that the earliest stages of the segmentation gene cascade established in Drosophila do not function in more ancestral insects. Exactly how short-germ-type embryos establish their segmental pattern remains to be discovered.